Arrested fungal biofilms as low-modulus structural bio-composites: Water holds the key

  • R. Aravinda NarayananEmail author
  • Asma Ahmed
Regular Article


Biofilms are self-assembling structures consisting of rigid microbial cells embedded in a soft biopolymeric extracellular matrix (ECM), and have been commonly viewed as being detrimental to health and equipment. In this work, we show that biofilms formed by a non-pathogenic fungus Neurospora discreta, are fungal bio-composites (FBCs) that can be directed to self-organize through active stresses to achieve specific properties. We induced active stresses by systematically varying the agitation rate during the growth of FBCs. By growing FBCs that are strong enough to be conventionally tensile loaded, we find that as agitation rate increases, the elongation strain at which the FBCs break, increases linearly, and their elastic modulus correspondingly decreases. Using results from microstructural imaging and thermogravimetry, we rationalize that agitation increases the production of ECM, which concomitantly increases the water content of agitated FBCs up to 250% more than un-agitated FBCs. Water held in the nanopores of the ECM acts a plasticizer and controls the ductility of FBCs in close analogy with polyelectrolyte complexes. This paradigm shift in viewing biofilms as bio-composites opens up the possibility for their use as sustainable, biodegradable, low-modulus structural materials.

Graphical abstract


Flowing Matter: Active Fluids 


  1. 1.
    H.C. Flemming, J. Wingender, Nat. Rev. Microbiol. 8, 623 (2010)CrossRefGoogle Scholar
  2. 2.
    A.P.J. Moore, D. Robson, G.D. Trinci, 21st Century Guidebook to Fungi (Cambridge University Press, Cambridge, UK, 2011)Google Scholar
  3. 3.
    J.N. Wilking, T.E. Angelini, A. Seminara, M.P. Brenner, D.A. Weitz, Mater. Res. Soc. 36, 385 (2011)CrossRefGoogle Scholar
  4. 4.
    M.G. Mazza, J. Phys. D: Appl. Phys. 49, 203001 (2016)ADSCrossRefGoogle Scholar
  5. 5.
    T. Shaw, M. Winston, C.J. Rupp, I. Klapper, P. Stoodley, Phys. Rev. Lett. 93, 98102 (2004)ADSCrossRefGoogle Scholar
  6. 6.
    V.D. Gordon, M. Davis-fields, K. Kovach, J. Phys. D: Appl. Phys. 50, 223002 (2017)ADSCrossRefGoogle Scholar
  7. 7.
    M. Morikawa, J. Biosci. Bioeng. 101, 1 (2006)CrossRefGoogle Scholar
  8. 8.
    B. Li, T.J. Webster, J. Orthop. Res. 36, 22 (2018)Google Scholar
  9. 9.
    C.C.C.R. De Carvalho, Front. Mar. Sci. 5, 1 (2018)CrossRefGoogle Scholar
  10. 10.
    N. Billings, A. Birjiniuk, T.S. Samad, P.S. Doyle, Rep. Prog. Phys. 78, 36601 (2015)CrossRefGoogle Scholar
  11. 11.
    M. Böl, A.E. Ehret, A. Bolea Albero, J. Hellriegel, R. Krull, Crit. Rev. Biotechnol. 33, 145 (2013)CrossRefGoogle Scholar
  12. 12.
    A. Ohashi, H. Harada, Water Sci. Technol. 29, 281 (1994)CrossRefGoogle Scholar
  13. 13.
    P. Stoodley, R. Cargo, C.J. Rupp, S. Wilson, I. Klapper, J. Ind. Microbiol. Biotechnol. 29, 361 (2002)CrossRefGoogle Scholar
  14. 14.
    D.N. Hohne, J.G. Younger, M.J. Solomon, Langmuir 25, 7743 (2009)CrossRefGoogle Scholar
  15. 15.
    F. Quiles, S. Saadi, G. Francius, J. Bacharouche, F. Humbert, Biochim. Biophys. Acta 1858, 75 (2016)CrossRefGoogle Scholar
  16. 16.
    S. Grumbein, M.W.O. Lieleg, S. Grumbein, M. Werb, J. Rheol. 60, 1085 (2016)ADSCrossRefGoogle Scholar
  17. 17.
    L.I. Brugnoni, M.C. Tarifa, J.E. Lozano, D. Genovese, Biofouling 30, 1269 (2014)CrossRefGoogle Scholar
  18. 18.
    H. Boudarel, J.D. Mathias, B. Blaysat, M. Grediac, Npj Biofilms Microbiomes 4, 17 (2018)CrossRefGoogle Scholar
  19. 19.
    Y.I. Yaman, E. Demir, R. Vetter, A. Kocabas, Nat. Commun. 10, 2285 (2018)ADSCrossRefGoogle Scholar
  20. 20.
    D.J. Wales, Energy Landscapes (Cambridge University Press, Cambridge, UK, 2003). Google Scholar
  21. 21.
    D. Needleman, Z. Dogic, Nat. Rev. Mater. 2, 17048 (2017)ADSCrossRefGoogle Scholar
  22. 22.
    S. Alexander, Phys. Rep. 296, 5 (1998)CrossRefGoogle Scholar
  23. 23.
    R. Hartmann, P.K. Singh, P. Pearce, R. Mok, B. Song, F. Díaz-Pascual, J. Dunkel, K. Drescher, Nat. Phys. 15, 251 (2019)CrossRefGoogle Scholar
  24. 24.
    J. Garcia-Ojalvo, Nat. Phys. 15, 207 (2019)CrossRefGoogle Scholar
  25. 25.
    K. Tai, M. Dao, S. Suresh, A. Palazoglu, C. Ortiz, Nat. Mater. 6, 454 (2007)ADSCrossRefGoogle Scholar
  26. 26.
    G. Tudryn, L. Schadler, R.C. Picu, M.R. Islam, R. Bucinell, Sci. Rep. 7, 1 (2017)CrossRefGoogle Scholar
  27. 27.
    M. Haneef, L. Ceseracciu, C. Canale, I.S. Bayer, J.A. Heredia-Guerrero, A. Athanassiou, Sci. Rep. 7, 41292 (2017)ADSCrossRefGoogle Scholar
  28. 28.
    A.J.T.M. Mathijssen, F. Guzmán-Lastra, A. Kaiser, H. Löwen, Phys. Rev. Lett. 121, 248101 (2018)ADSCrossRefGoogle Scholar
  29. 29.
    H.J. Vogel, Am. Nat. XCVIII, 435 (1964)CrossRefGoogle Scholar
  30. 30.
    R. Rezakhaniha, A. Agianniotis, J.T.C. Schrauwen, A. Griffa, D. Sage, C.V.C. Bouten, F.N. Van De Vosse, M. Unser, N. Stergiopulos, Biomech. Model. Mechanobiol. 11, 461 (2012)CrossRefGoogle Scholar
  31. 31.
    A. Heydorn, A.T. Nielsen, M. Hentzer, M. Givskov, B.K. Ersbøll, S. Molin, Microbiology 146, 2395 (2000)CrossRefGoogle Scholar
  32. 32.
    P. Stoodley, R. Cargo, C.J. Rupp, S. Wilson, I. Klapper, J. Ind. Microbiol. Biotechnol. 29, 361 (2002)CrossRefGoogle Scholar
  33. 33.
    W.D. Comper, R.P.W. Williams, O. Zamparo, Connect. Tissue Res. 25, 89 (1990)CrossRefGoogle Scholar
  34. 34.
    P.S. Stewart, J. Bacteriol. 185, 1485 (2003)CrossRefGoogle Scholar
  35. 35.
    C.P. Peter, Y. Suzuki, J. Bu, Biotechnol. Bioeng. 93, 1164 (2006)CrossRefGoogle Scholar
  36. 36.
    P. Ghosh, J. Mondal, E. Ben-Jacob, H. Levine, Proc. Natl. Acad. Sci. U.S.A. 112, E2166 (2015)ADSCrossRefGoogle Scholar
  37. 37.
    E. Paramonova, B.P. Krom, H.C. van der Mei, H.J. Busscher, P.K. Sharma, Microbiology 155, 1997 (2009)CrossRefGoogle Scholar
  38. 38.
    H.H. Hariri, J.B. Schlenoff, Macromolecules 43, 8656 (2010)ADSCrossRefGoogle Scholar
  39. 39.
    H.H. Hariri, A.M. Lehaf, J.B. Schlenoff, Macromolecules 45, 9364 (2012)ADSCrossRefGoogle Scholar
  40. 40.
    D. De Beer, P. Stoodley, Z. Lewandowski, Biotechnol. Bioeng. 44, 636 (1994)CrossRefGoogle Scholar
  41. 41.
    A. Birjiniuk, N. Billings, E. Nance, J. Hanes, K. Ribbeck, P.S. Doyle, New J. Phys. 16, 85014 (2014)CrossRefGoogle Scholar
  42. 42.
    H.C. Flemming, J. Wingender, Nat. Rev. Microbiol. 8, 623 (2010)CrossRefGoogle Scholar
  43. 43.
    M. Rubinstein, R.H. Colby, Polymer Physics (Oxford University Press, New York, 2003)Google Scholar
  44. 44.
    L.R. Madden, D.J. Mortisen, E.M. Sussman, S.K. Dupras, J.A. Fugate, J.L. Cuy, K.D. Hauch, M.A. Laflamme, C.E. Murry, B.D. Ratner, Proc. Natl. Acad. Sci. U.S.A. 107, 15211 (2010)ADSCrossRefGoogle Scholar
  45. 45.
    A. Mohamed El-hadi, H. Alamri, Polymers 10, 1174 (2018)CrossRefGoogle Scholar
  46. 46.
    R. Mandal, P.J. Bhuyan, P. Chaudhuri, M. Rao, C. Dasgupta, Phys. Rev. E 96, 42605 (2017)ADSCrossRefGoogle Scholar

Copyright information

© EDP Sciences, Società Italiana di Fisica and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of PhysicsBirla Institute of Technology and Science (Pilani)HyderabadIndia
  2. 2.School of Human and Life SciencesCanterbury Christ Church UniversityCanterburyUK

Personalised recommendations